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Download Author Version (PDF) RSC Advances This is an Accepted Manuscript, which has been through the Royal Society of Chemistry peer review process and has been accepted for publication. Accepted Manuscripts are published online shortly after acceptance, before technical editing, formatting and proof reading. Using this free service, authors can make their results available to the community, in citable form, before we publish the edited article. This Accepted Manuscript will be replaced by the edited, formatted and paginated article as soon as this is available. You can find more information about Accepted Manuscripts in the Information for Authors. Please note that technical editing may introduce minor changes to the text and/or graphics, which may alter content. The journal’s standard Terms & Conditions and the Ethical guidelines still apply. In no event shall the Royal Society of Chemistry be held responsible for any errors or omissions in this Accepted Manuscript or any consequences arising from the use of any information it contains. www.rsc.org/advances Page 1 of 31 RSC Advances Fungal-bacterial interactions in mice with dextran sulfate sodium (DSS)-induced acute and chronic colitis Xinyun Qiu 1, 2# , Xia Li 1, Zhe Wu 1, Feng Zhang 1, Ning Wang 1, Na Wu 3, Xi Yang 4, Yulan Liu 1* . 1Department of Gastroenterology, Peking University People's Hospital, Beijing, China. Manuscript 2 Department of Gastroenterology, First Affiliated Hospital of Nanjing Medical University, Nanjing, China. 3Institute of Clinical Molecular Biology & Central Laboratory, Peking University People's Hospital, Beijing, China. Accepted 4 CAS Key Laboratory of Pathogenic Microbiology and Immunology, Institute of Micro-biology, Chinese Academy of Sciences, Beijing, China. # Dr. Xinyun Qiu is a doctoral candidate in Department of Gastroenterology, Peking University People's Hospital from September 2012 to July 2015, and now he is a resident physician in Department of Gastroenterology, First Affiliated Hospital of Nanjing Medical University. Advances *Corresponding author. Mailing address for Yulan Liu: RSC Department of Gastroenterology, Peking University People's Hospital No. 11 Xizhimen South Street, Xicheng District, Beijing 100044, China. Phone: (8610)8832-5559; Fax: (8610)6831-8386; E-mail: [email protected] RSC Advances Page 2 of 31 Running Title: Fungal-bacterial interactions in mice with DSS-colitis. ABSTRACT The commensal intestinal microbiota plays critical roles in the initiation and development of Manuscript inflammatory bowel diseases (IBD). However, the importance of intestinal fungi and their interactions with bacteria in the pathogenesis of IBD is unclear. In this study, anti-fungal drugs (fluconazole or Amphotericin B [AmpB]) were administered to control mice and those treated, acutely (A-DSS) and chronically (C-DSS) with DSS. The severity of colonic inflammation was assessed, and Accepted pro-inflammatory cytokine levels in the colonic mucosa and serum were detected by real-time PCR and multiplex ELISA assay, respectively. The colonic bacterial 16S rDNA V3 region was analysed in normal and anti-fungal drug-treated mice by pyrosequencing. Specific bacterial genera related to IBD, butyryl-CoA/acetate-CoA transferase (a key transferase for butyrate production in bacteria) and tight-junction proteins (occludin and ZO-1) in the colonic mucosa were detected by real-time PCR Advances and/or western blot. The results showed that compared with controls ，intestinal Bacteroides , Alistipes , and Lactobacillus were increased in fluconazole treated mice; while only Alistipes was increased in AmpB treated mice. Clostridium cluster XIVa and butyryl-CoA/acetate-CoA transferase levels were RSC reduced in both groups. Treatment with a high dose of anti-fungal drugs dampened colonic occludin and ZO-1, aggravated A-DSS colitis, and exhibited no beneficial role in C-DSS colitis. However, reducing fluconazole concentration to an appropriate dose attenuated C-DSS colitis. In conclusion, fungi are important co-operators with bacteria in maintaining intestinal micro-ecological equilibrium. Extensive Page 3 of 31 RSC Advances clearance of gut fungi could disrupt intestinal bacterial homeostasis and have an adverse impact on IBD. Studies investigating the intestinal fungal-bacterial interactions would aid the appropriate use of anti-fungal drugs in treating IBD. Key words: Inflammatory bowel disease, Colitis, Intestinal microbiota, Fungi, Fungal-bacterial interactions. BACKGROUND Inflammatory bowel diseases (IBDs) such as ulcerative colitis (UC) and Crohn’s disease (CD), are caused by multiple factors, including genetics, environment, immune dysfunction, and disturbance Manuscript of the intestinal microbiota. The latter comprises a large and diverse community of bacteria, fungi, viruses, and archaea 1. The intestinal microbiota plays vital roles in developing and maintaining host immunology, physiology, nutrition, and metabolism 2. Patients with IBD are usually characterised by disturbances in their intestinal microflora. Accepted Several studies have reported an increased abundance of Gammaproteobacteria and Enterobacteriaceae , and decreased abundance of Firmicutes in both UC and CD patients 3-5. Numbers of bacteria producing butyrate, an important short chain fatty acid (SCFA) that plays a major role in promoting visceral function and integrity, are significantly decreased in the gut of IBD patients 6, 7. Additionally, pathogenic sulfur-reducing, bile-tolerant bacteria, which produce toxic and Advances proinflammatory hydrogen sulfide and exacerbate intestinal inflammation, are increased in the gut of UC patients 8, 9. Besides bacteria, intestinal fungi also exhibit a significant change during inflammatory condition. Denaturing gradient gel electrophoresis analysis of fungal 18S rDNA showed different RSC fungal profiles between UC patients and healthy individuals, and an increased proportion of Candida albicans was found in the colons of CD patients 10 , 11 , causing aggravated mucosal injury and generation of anti-Saccharomyces cerevisiae antibodies (ASCA) 12-14 . Pathogenic gut microbiota could be an important inducer in IBD initiation and perpetuation, and RSC Advances Page 4 of 31 past studies have verified that elimination of gut bacteria by broad-spectrum antibiotics is effective in inducing IBD remission 15 . However, to our knowledge, the role of anti-fungal drugs in treating IBD has not been demonstrated conclusively. Fungi and bacteria coexist in the gastro-intestinal (GI) canal, where they interact extensively with each other 16 , 17 . Fungi usually bloom during antibiotic perturbations, especially in immunocompromised patients such as those with acquired immune deficiency syndrome (AIDS), some cancers, and transplant recipients 18 . Dollive et al 18 demonstrated an outgrowth of fungi in both short-term and long-term antibiotic treatment in mouse models and found that Candida can persist in the gut at a high level for eight weeks after the cessation of antibiotics. However, whether anti-fungal drugs have an effect on intestinal bacteria is unknown. The objective of this study was to elucidate the interactions between intestinal bacteria and fungi, Manuscript and to investigate the role of intestinal fungi in IBD. To this end, we investigated the effects of anti-fungal drugs (fluconazole and amphotericin B [AmpB]) in dextran sulphate sodium (DSS)-induced murine acute and chronic IBD models, and compared the bacterial composition in the colonic mucosa between normal and anti-fungal drug-treated mice. Our results unravel the interaction between bacteria and fungi in the gut and further our knowledge of microbial homeostasis in the GI Accepted canal. MATERIALS AND METHODS Animal protocols Advances Six-week-old C57B/L6J mice were purchased from the Experimental Animal Center, Academy of Military Medical Sciences (Beijing, China), housed four to five per cage and placed on standardized RSC rodent food and distilled water for four weeks prior to the study to stabilize their microflora. To induce acute DSS-colitis, mice were given drinking water containing 2.5% (w/v) DSS (MP Biomedicals, Aurora, OH) ad libitum for seven days and distilled water for two additional days before sacrifice. To induce chronic DSS-colitis, mice were given four cycles of 7-day 2.5% (w/v) DSS followed by 7-day Page 5 of 31 RSC Advances water (DSS+water) treatment 19 (Figure S1). All animal experiments were approved by the Committee for Laboratory Animal Management of Peking University and treated humanely according to the National Institutes of Health guidelines on the ethical use of animals. Effect of anti-fungal drugs in mice with acute-DSS (A-DSS) colitis To induce acute DSS-colitis (A-DSS), mice were given water containing 2.5% (w/v) DSS (molecular weight 36–50 kDa; MP Biomedicals) ad libitum for seven days followed by water without DSS for two additional days before sacrifice. Two anti-fungal drugs (fluconazole and AmpB) were tested in the A-DSS model in separate experiments. In the first experiment, animals were divided into the Manuscript following four treatment groups (n = 8–10 per group): normal, A-DSS, fluconazole, and A-DSS + fluconazole. In the second experiment, the same groups were used, but fluconazole was replaced with AmpB. To deplete intestinal fungi using fluconazole, the fluconazole and A-DSS + fluconazole groups were exposed to fluconazole (0.5 mg/mL, Sigma-Aldrich, St Louis, MO) via their drinking water 20 on days 1–23. In the A-DSS and A-DSS + fluconazole groups, 2.5% (w/v)
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